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Chordotonal organs in hemipteran insects: unique peripheral structures but conserved central organization revealed by comparative neuroanatomy

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Abstract

Hemipteran insects use sophisticated vibrational communications by striking body appendages on the substrate or by oscillating the abdominal tymbal. There has been, however, little investigation of sensory channels for processing vibrational signals. Using sensory nerve stainings and low invasive confocal analyses, we demonstrate the comprehensive neuronal mapping of putative vibration-responsive chordotonal organs (COs) in stink bugs (Pentatomidae and Cydinidae) and cicadas (Cicadidae). The femoral CO (FCO) in stink bugs consists of ventral and dorsal scoloparia, homologous to distal and proximal scoloparia in locusts, which are implicated in joint movement detection and vibration detection, respectively. The ligament of the dorsal scoloparium is distally attached to the accessory extensor muscle, whereas that of the ventral scoloparium is attached to a specialized tendon. Their afferents project to the dorso-lateral neuropil and the central region of the medial ventral association center (mVAC) in the ipsilateral neuromere, where presumed dorsal scoloparium afferents and subgenual organ afferents are largely intermingled. In contrast, FCOs in cicadas have decreased dorsal scoloparium neurons and lack projections to the mVAC. The tymbal CO of stink bugs contains four sensory neurons that are distally attached to fat body cells via a ligament. Their axons project intersegmentally to the dorsal region of mVACs in all neuromeres. Together with comparisons of COs in different insect groups, the results suggest that hemipteran COs have undergone structural modification for achieving faster signaling of resonating peripheral tissues. The conserved projection patterns of COs suggest functional importance of the FCO and subgenual organ for vibrational communications.

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Abbreviations

abCO:

Abdominal chordotonal organ

AEM:

Accessory extensor muscle

AN:

Auditory nerve

CG:

Central ganglion

CNS:

Central nervous system

CO:

Chordotonal organ

DC:

Descending connective

DET:

Distal extensor tendon

DL:

Dorsal ligament

DS:

Dorsal scoloparium

FCO:

Femoral chordotonal organ

F-T Joint:

femoro-tibial joint

JO:

Johnston’s organ

MLN:

Main leg nerve

PG:

Prothoracic ganglion

PES:

Proximal extracellular space

PlCO:

Pleural CO

SC:

Scolopale cap

SEG:

Subesophageal ganglion

Sep:

Septum

SGO:

Subgenual organ

SR:

Strand receptor

tyCO:

Tymbal CO

TeN:

Tensor nerve

TEPS:

Tibial extensor pendant sclerite

TyN:

Tymbal nerve

VL:

Ventral ligament

VS:

Ventral scoloparium

WGA:

Wheat germ agglutinin

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Acknowledgments

This work was supported by Innovative Materials Engineering Based on Biological Diversity in Grant-in-Aid for Scientific Research on Innovative Areas (project number: 80332477) to HN and TT, Council for Science, Technology and Innovation, Cross-ministerial Strategic Innovation Promotion Program to TT and Grant-in-Aid for JSPS Fellow (14 J30005) and Young Scientists (B) (15 K18618) to HM. We thank K. Katoh for collecting L. bihamatus, Dr. T. Ichikawa (Kyusyu University) for supplying Z. atratus and Drs. T. Ishikawa (Tokyo University of Agriculture), Niels Skals (University of Copenhagen) and two anonymous reviewers for comments on the manuscript.

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  1. Research Institute for Electronic Science, Hokkaido University, Sapporo, 060-0812, Japan

    Hiroshi Nishino

  2. Department of Forest Entomology, Forestry and Forest Products Research Institute, Matsuno-sato 1, Tsukuba, Ibaraki, 305-8687, Japan

    Hiromi Mukai & Takuma Takanashi

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  1. Hiroshi Nishino
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Correspondence to Hiroshi Nishino.

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Fig. S1

Staining procedures. (a, b) Examples of retrograde staining of the main leg nerve (MLN) with microruby in P. stali (a) and NiCl2 (reacted with rubeanic acid) in P. Japonensis (b). c An example of anterograde staining of three peripheral nerves with microruby to label their axon terminalss in the central ganglion (CG). d An unfixed central ganglion reacted with rubeanic acid in which the tymbal nerve (left) and the metathoracic MLN (right) were retrogradely labeled with NiCl2. PG prothoracic ganglion. e–g Fat body cells in the body lumen of P. stali at low (e), mid- (f) and high magnifications (g, stained with toluidine blue). Scale bars (a, b, e) 1 mm; (c, f) 500 μm; (d) 200 μm; (g) 20 μm. (GIF 437 kb)

High resolution image (TIF 12863 kb)

Fig. S2

Anterograde labeling of four nerves innervating the proximal region of the abdomen. a Nomenclature of peripheral nerves in the central ganglion (CG). b–g Projections of N1 (b), N2 (c) and N3 (d) indicating one or two CO afferents projecting to the mVAC for each nerve. They have no axons that ascend to the brain. h–l Projections of the tymbal nerve (TN) showing four CO afferents (indicated by black arrows in h and i) in prothoracic (j), mesothoracic (k) and metathoracic neuromeres (l). Two CO afferents have collaterals that terminate in the antennal mechanosensory and motor center in the brain (indicated by yellow arrows in h and i). See Fig. 7 for details. Scale bars (b–g) 100 μm; (h, i) 200 μm; (j–l) 50 μm. (GIF 535 kb)

High resolution image (TIF 12.8 mb)

Fig. S3

Projection patterns of two populations of abdominal COs. a, b Anterograde staining of the most peripheral dorsal branch of the primary nerve in the fifth abdominal segment, showing projections of hair receptors confined to the most ventral neuropil. c, d Anterograde staining of the nerve branch innervating the pleural CO in the fifth (left) and sixth abdominal segments showing a single afferent that has collaterals in the dorsal region of mVACs in the meso- and metathoracic neuromeres (d) and terminate in the prothoracic neuromere. e-h, Anterograde staining of the distal tip of the nerve containing only the pleural CO (right, g) and more proximal nerve branch containing only ventral COs (e, f) ventral COs, revealing that the ventral CO has localized branches in the metathoracic neuromere. Scale bars (a, c, e, g) 100 μm; (b, d, f, h) 50 μm. (GIF 627 kb)

High resolution image (TIF 17346 kb)

Fig. S4

Retrograde labeling of prothoracic FCO neurons (magenta) and surrounding structures (green) in P. stali, viewed anteriorly. (AVI 6428 kb)

Fig. S5

Retrograde labeling of prothoracic FCO neurons (magenta) and F-action filaments (green) in P. Japonensis showing different scolopale structures of dorsal scoloparium neurons (surrounded by white line) and ventral scoloparium neurons. (AVI 2256 kb)

Fig. S6

Anterograde labeling of the main metathoracic leg nerve (green) and the tymbal nerve (magenta) in P. stali showing projections of FCO/SGO afferents (green) and tymbal CO afferents (magenta) to the mVAC, viewed anteriorly. (AVI 2976 kb)

Fig. S7

Anterograde labeling of the auditory nerve (left, magenta) and tensor nerve (left, green) and the main metathoracic leg nerve (right, green) in L. bihamatus showing that auditory nerve afferents are more dorsally located than tensor nerve afferents in the mVAC and that metathoracic FCO afferents do not enter the mVAC. (AVI 5763 kb)

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Nishino, H., Mukai, H. & Takanashi, T. Chordotonal organs in hemipteran insects: unique peripheral structures but conserved central organization revealed by comparative neuroanatomy. Cell Tissue Res 366, 549–572 (2016). https://doi.org/10.1007/s00441-016-2480-0

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